Alterations in acetylcholine release in the rat hippocampus during sleep-wakefulness detected by intracerebral dialysis

Kametani, Hideki; Kawamura, Hiroshi

doi:10.1016/0024-3205(90)90300-g

Cited by 120 publications

(92 citation statements)

References 14 publications

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“…Thus, conceptually, it seems an ingredient crucial for a system able to predict. The differential modulation of collateral connections in encoding and retrieval has been discussed extensively by Hasselmo et al (1996) as a possible function of acetylcholine; though our mechanism A2 would require collaterals in CA3 to be suppressed at retrieval, contrary to experimental evidence (Kametani and Kawamura, 1990;Hasselmo et al, 1995;Marrosu et al, 1995)-and, indeed, its implausibility is matched by its failure to generate a predictive ability.…”

mentioning

confidence: 60%

Computational constraints between retrieving the past and predicting the future, and the CA3‐CA1 differentiation

Treves

2004

Hippocampus

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ABSTRACT:The differentiation between the CA3 and CA1 fields of the mammalian hippocampus is one of the salient traits that set it apart from the organization of the homologue medial wall in reptiles and birds. CA3 is widely thought to function as an autoassociator, but what do we need CA1 for? Based on evidence for a specific role of CA1 in temporal processing, I have explored the hypothesis that the differentiation between CA3 and CA1 may help solve a computational conflict. The conflict is between pattern completion, or integrating current sensory information on the basis of memory, and prediction, or moving from one pattern to the next in a stored sequence. CA3 would take care of the former, while CA1 would concentrate on the latter. I have found the hypothesis to be only weakly supported by neural network simulations. The conflict indeed exists, but two mechanisms that would relate more directly to a functional CA3-CA1 differentiation were found unable to produce genuine prediction. Instead, a simple mechanism based on firing frequency adaptation in pyramidal cells was found to be sufficient for prediction, with the degree of adaptation as the crucial parameter balancing retrieval with prediction. The differentiation between the architectures of CA3 and CA1 has a minor but significant, and positive, effect on this balance. In particular, for a fixed anticipatory interval in the model, it increases significantly the information content of hippocampal outputs. There may therefore be just a simple quantitative advantage in differentiating the connectivity of the two fields. Moreover, different degrees of adaptation in CA3 and CA1 cells were not found to lead to better performance, further undermining the notion of a functional dissociation.

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confidence: 60%

Computational constraints between retrieving the past and predicting the future, and the CA3‐CA1 differentiation

Treves

2004

Hippocampus

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“…The neuromodulator profile of REM sleep reveals a powerful boost in acetylcholine, combined with a diminished role of norepinephrine and serotonin (55). In fact, REM sleep has been shown to have the highest levels of cortical acetylcholine compared with active wake, quiet wake, and NREM sleep (56)(57)(58)(59). Acetylcholine allows for induction and maintenance of long-term potentiation (60,61), which is considered a possible mechanism of synaptic plasticity in implicit learning (62).…”

Section: Discussionmentioning

confidence: 99%

Autonomic activity during sleep predicts memory consolidation in humans

Whitehurst

Cellini

McDevitt

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Throughout history, psychologists and philosophers have proposed that good sleep benefits memory, yet current studies focusing on the relationship between traditionally reported sleep features (e.g., minutes in sleep stages) and changes in memory performance show contradictory findings. This discrepancy suggests that there are events occurring during sleep that have not yet been considered. The autonomic nervous system (ANS) shows strong variation across sleep stages. Also, increases in ANS activity during waking, as measured by heart rate variability (HRV), have been correlated with memory improvement. However, the role of ANS in sleepdependent memory consolidation has never been examined. Here, we examined whether changes in cardiac ANS activity (HRV) during a daytime nap were related to performance on two memory conditions (Primed and Repeated) and a nonmemory control condition on the Remote Associates Test. In line with prior studies, we found sleep-dependent improvement in the Primed condition compared with the Quiet Wake control condition. Using regression analyses, we compared the proportion of variance in performance associated with traditionally reported sleep features (model 1) vs. sleep features and HRV during sleep (model 2). For both the Primed and Repeated conditions, model 2 (sleep + HRV) predicted performance significantly better (73% and 58% of variance explained, respectively) compared with model 1 (sleep only, 46% and 26% of variance explained, respectively). These findings present the first evidence, to our knowledge, that ANS activity may be one potential mechanism driving sleep-dependent plasticity.sleep | heart rate variability | memory | consolidation | vagal activity S leep has been shown to facilitate the transformation of recent experiences into stable, long-term memories (i.e., consolidation), and specific electrophysiological sleep features have been implicated in this process (1). For example, minutes spent in slow wave sleep (SWS) and the number of sleep spindles [transient neural events in nonrapid eye movement (NREM) sleep, 12-15 Hz] in a posttraining sleep period correlate with the magnitude of explicit memory improvement [e.g., conscious, episodic memories (2, 3)]. Minutes in rapid eye movement (REM) sleep, on the other hand, are associated with improvements in implicit memory [e.g., unconscious, priming, procedural skills (4, 5)]. However, recent reviews and meta-analyses of the literature report inconsistencies in these findings (6, 7), suggesting that there may be unexplored factors critical to sleep-dependent memory consolidation.One possible influence that has received little attention in the sleep and memory literature is the autonomic nervous system (ANS). This lack of attention is somewhat surprising, considering that the literature describing ANS modulation of memory during wake is well established (8). Studies have found that memory storage of new information can be enhanced or impaired by directly modifying the activity of peripheral hormones following acquisition (9...

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“…The ACF was used to present tones only when the subject was in a state of quiet waking as determined by regular respiration; the ACF criterion was 80% of a perfect sinusoid for a period of 4 s. Trials meeting this criterion were presented if the scheduled intertrial interval period had passed (30-180 s). This state control was employed to avoid giving stimuli when very high levels of ACh were being released in the cortex, as during exploration or REM sleep (Giovannini, Rakovska, Benton, Pazzagli, Bianchi, & Pepeu, 2001;Jasper & Tessier, 1971;Kametani & Kawamura, 1990;Marrosu, Portas, Mascia, Casu, Fa, Giagheddu, Imperato, & Gessa, 1995) to prevent a ceiling effect, thus promoting a physiologically-effective release of ACh by NBstm.…”

Section: Induction Of Memory: Stimuli Recording and Data Analysismentioning

confidence: 99%

Motivationally neutral stimulation of the nucleus basalis induces specific behavioral memory

Miasnikov

Chen

Gross

et al. 2008

Neurobiology of Learning and Memory

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The cholinergic system has been implicated in learning and memory. The nucleus basalis (NB) provides acetylcholine (ACh) to the cerebral cortex. Pairing a tone with NB stimulation (NBstm) to alter cortical state induces both associative specific tuning plasticity in the primary auditory cortex (A1) and associative specific auditory behavioral memory. NB-induced memory has major features of natural memory that is induced by pairing a tone with motivational reinforcers, e.g., food or shock, suggesting that the cholinergic system may be a "final common pathway" whose activation promotes memory storage. Alternatively, NB-stimulation might itself be motivationally significant, either rewarding or punishing. To investigate these alternatives, adult male rats (n = 7) first formed a specific NB-induced memory (CS = 8.0 kHz, 2.0 s paired with NBstm, ISI = 1.8 s, 200 trials), validated by post-training (24 h) frequency generalization gradients (1-15 kHz) of respiration interruption that were specific to the CS frequency. Thereafter, they received the same level of NBstm that had induced memory, while confined to one quadrant of an arena, and later tested for place preference, i.e., avoidance or seeking of the quadrant of NBstm. This NBstm group exhibited neither preference for nor against the stimulated quadrant, compared to sham-operated subjects (n = 7). The findings indicate that specific associative memory can be induced by direct activation of the NB without detectable motivational effects of NB stimulation. These results are concordant with a memorypromoting role for the nucleus basalis that places it "downstream" of motivational systems, which activate it to initiate the storage of the current state of its cholinergic targets.

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Alterations in acetylcholine release in the rat hippocampus during sleep-wakefulness detected by intracerebral dialysis

Cited by 120 publications

References 14 publications

Computational constraints between retrieving the past and predicting the future, and the CA3‐CA1 differentiation

Computational constraints between retrieving the past and predicting the future, and the CA3‐CA1 differentiation

Autonomic activity during sleep predicts memory consolidation in humans

Motivationally neutral stimulation of the nucleus basalis induces specific behavioral memory

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